Chapter 7 Plasticity of Communication in Nonhuman Primates

Humans and other primates communicate in multiple sensory modalities, and language itself is usually a multimodal form of communication. Discussion of the multimodal nature of primate communication goes back at least as far as the publications of Charles Darwin and has recently seen renewed interest. Here, I review key topics in the study of multimodal communication in nonhuman primates and humans, including issues of definitional complexity as well as classification systems and empirical approaches. I argue that multimodal communication is ubiquitous, ingrained, and advantageous. I discuss sensory aging and how multimodal communication can offer alternative routes to comprehension when sensory systems become impaired. To conclude, I consider future avenues of research that seem likely to prove productive.

In searching for the roots of human language, comparative researchers investigate whether precursors to language are already present in our closest relatives, the non-human primates. As the majority of studies into primates’ communication use a unimodal approach with focus on one signal type only, researchers investigate very different aspects depending on whether they are interested in vocal, gestural, or facial communication. Here, we focus on two signal types and discuss how meaning is created in the gestural (visual, tactile/auditory) as compared to the vocal modality in non-human primates, to highlight the different research foci across these modalities. First, we briefly describe the defining features of meaning in human language and introduce some debates concerning meaning in non-human communication. Second, with focus on these features, we summarize the current evidence for meaningful communication in gestural as compared to vocal communication and demonstrate that meaning is operationalized very differently by researchers in these two fields. As a result, it is currently not possible to generalize findings across these modalities. Rather than arguing for or against the occurrence of semantic communication in non-human primates, we aim at pointing to gaps of knowledge in studying meaning in our closest relatives, and these gaps might be closed.

There is growing evidence that activation of the motor system during observation of actions, a phenomenon first observed in non-human primates, underlies action understanding and even communication. This review (a) examines the evidence on motor system activity as an underlying neural correlate of action understanding; (b) reviews the theoretical and empirical work linking action understanding and the development of communication, with a specific focus on the role that gestures play as an intermediary; and (c) discusses the research on and existing opportunities for understanding the link between the motor system and communication in both humans and non-human primates, through the lens of action perception. Bringing together findings and perspectives from developmental social cognition in both humans and non-human primates and applying recent neuroscientific perspectives will help to elucidate the processes underlying the ability to understand and communicate with others.

Medial prefrontal cortices in primates have been associated with emotion, memory, and complex cognitive processes. Here we investigated whether the pattern of cortical connections could indicate whether the medial prefrontal cortex constitutes a homogeneous region, or if it can be parceled into distinct sectors. Projections from medial temporal memory-related cortices subdivided medial cortices into different sectors, by targeting preferentially caudal medial areas (area 24, caudal 32 and 25), to a lesser extent rostral medial areas (rostral area 32, areas 14 and 10), and sparsely area 9. Area 9 was distinguished by its strong connections with premotor cortices. Projections from unimodal sensory cortices reached preferentially specific medial cortices, including a projection from visual cortices to area 32/24, from somatosensory cortices to area 9, and from olfactory cortices to area 14. Medial cortices were robustly interconnected, suggesting that local circuits are important in the neural processing in this region. Medial prefrontal cortices were unified by bidirectional connections with superior temporal cortices, including auditory areas. Auditory pathways may have a role in the specialization of medial prefrontal cortices in species-specific communication in non-human primates and language functions in humans.

Social communication in nonhuman primates and humans is strongly affected by facial information from other individuals. Many cortical and subcortical brain areas are known to be involved in processing facial information. However, how the neural representation of faces differs across different brain areas remains unclear. Here, we demonstrate that the reference frame for spatial frequency (SF) tuning of face-responsive neurons differs in the temporal visual cortex and amygdala in monkeys. Consistent with psychophysical properties for face recognition, temporal cortex neurons were tuned to image-based SFs (cycles/image) and showed viewing distance-invariant representation of face patterns. On the other hand, many amygdala neurons were influenced by retina-based SFs (cycles/degree), a characteristic that is useful for social distance computation. The two brain areas also differed in the luminance contrast sensitivity of face-responsive neurons; amygdala neurons sharply reduced their responses to low luminance contrast images, while temporal cortex neurons maintained the level of their responses. From these results, we conclude that different types of visual processing in the temporal visual cortex and the amygdala contribute to the construction of the neural representations of faces.

Facial displays are an important form of social communication in nonhuman primates. Clues to the information conveyed by faces are the temporal and spatial characteristics of ocular viewing patterns to facial images. The present study compares viewing patterns of four rhesus monkeys (Macaca mulatta) to a set of 1- and 3-sec video segments of conspecific facial displays, which included open-mouth threat, lip-smack, yawn, fear-grimace, and neutral profile. Both static and dynamic video images were used. Static human faces displaying open-mouth threat, smile, and neutral gestures were also presented. Eye position was recorded with a surgically implanted eye-coil. The relative perceptual salience of the eyes, the midface, and the mouth across different expressive gestures was determined by analyzing the number of eye movements associated with each feature during static and dynamic presentations. The results indicate that motion does not significantly affect the viewing patterns to expressive facial displays, and when given a choice, monkeys spend a relatively large amount of time inspecting the face, especially the eyes, as opposed to areas surrounding the face. The expressive nature of the facial display also affected viewing patterns in that threatening and fear-related displays evoked a pattern of viewing that differed from that recorded during the presentation of submissive-related facial displays. From these results we conclude that (1) the most important determinant of the visual inspection patterns of faces is the constellation of physiognomic features and their configuration, but not facial motion, (2) the eyes are generally the most salient facial feature, and (3) the agonistic or affiliative dimension of an expressive facial display can be delineated on the basis of viewing patterns.

Auditory, visual and olfactory cues play varying roles in non-human primate communication, and these systems have been intensively studied over the last several decades. The use of vocalisations as a primary mode of communication has been the focus of much research, especially in attempts to understand the origins of human language, with a major focus on anthropoid primates and diurnal lemurs. Over the last decade, technological advances have allowed researchers to begin to conduct in-depth investigations into the communication systems exhibited by the nocturnal and cathemeral prosimian primates, including tarsiers, lemurs and lorises. Understanding how nocturnal prosimians use visual, olfactory and auditory cues is vital for reconstructing the origins of primate communication systems. In this special issue, we highlight some of the more exciting advances in the communication strategies of the prosimians. Contributions come from work conducted in Kenya, Tanzania, Senegal, Rwanda, Madagascar and the Indonesian islands of Java and Sulawesi. Topics will include: the description of novel ultrasonic vocalisations, including frequency and function of these newly discovered calls; the possible use of vocalisations to navigate and assemble at sleep sites; the importance of species-specific contact vocalisations for the identification of new species; the use of urinary and glandular signals to communicate and the methods developed to understand this complex communication in the field; the use of vocalisations for niche separation among nocturnal primates from mainland Africa and Madagascar; and whether or not we can use new technologies to discern whether prosimians use vocalisations for individual identification of group members. We discuss the importance of new field methods including novel equipment and techniques, the use of vocalisation to influence conservation practices and the importance of comparing across prosimian taxa to reconstruct the communication systems of our early primate ancestors.

Evolutionary changes to the primate skull and dentition: C. L. B. Lavelle, R. P. Shellis, and D. F. G. PooleSpringfield, Ill., 1977, Charles C Thomas Publisher. 285 pages, illustrated

Gestural Communication in Human and Non-Human Primates

Ackermann et al. outline a model for elaboration of subcortical motor outputs as a driving force for the development of the apparently unique behaviour of language in humans. They emphasize circuits in the striatum and midbrain, and acknowledge, but do not explore, the importance of the auditory perceptual pathway for evolution of verbal communication. We suggest that understanding the evolution of language will also require understanding of vocalization perception, especially in the auditory cortex.

Communication between humans and nonhuman animals has been complicated by traditional assumptions that human language is preeminent. While some anthropologists have explored communication in nonhuman primates to inform our understanding of the evolution of human language, there has been reluctance within sociocultural anthropology to consider the communicative competencies of other species as intrinsically valuable. However, spoken language is just one of many communicative forms. Other animals also possess complex systems of communication, some displaying social aspects of human discourse such as turn‐taking, and some with such requisite criteria for language as a shared system of representational signs. Nonverbal communication is another feature of human and nonhuman social life, facilitating trans‐species empathy, while in systems of communication which utilize capacities humans lack, the precise meanings and mechanisms currently elude human understanding. This entry presents some representative examples of nonhuman and of human–nonhuman communication systems in relation to assumptions about human language.

The alarm calls of nonhuman primates are occasionally cited as functionally equivalent to lexical word meaning in human language. Recently, however, it has become increasingly unlikely that one-to-one relations between alarm call structures and predator categories are the default, mainly because many call types are produced in multiple contexts, requiring more complex notions of meaning. For example, male vervet monkeys produce the same alarm calls during encounters with terrestrial predators and neighbouring groups, suggesting that recipients require additional information to attribute meaning to the calls. We empirically tested the hypothesis that vervet monkeys take contextual information into account when responding to each other's alarm calls. In playback experiments, we exposed subjects to recordings of male alarm barks during actual intergroup encounters (predator unlikely) or when there was no intergroup encounter (predator likely). Subjects responded more strongly in the no intergroup encounter situations, typically associated with discovering a hiding predator, measured in terms of startle responses, vigilance behaviour and gazing towards the presumed caller. We discuss the significance of using contextual information for meaning attribution in nonhuman primate communication.

A developing body of research suggests that there are few sex differences in the rate and severity of problem behavior in early childhood, but clear sex differences emerge at about 4 years of age. The authors explore 2 hypotheses to further the understanding of emerging sex differences in problem behavior across the first 5 years of life. The first posits that the change in girls' problem behavior from infancy to school entry represents a channeling of early problem behavior into predominantly internalizing problems as a result of socialization. The second hypothesis is that the change in girls' early problem behavior during the preschool period results from the more rapid biological, cognitive, and social-emotional development of girls relative to boys. The authors review research on the influence of parents, teachers, and peers on girls' behavior from infancy to preschool regarding the first hypothesis, whereas they review studies of sex differences in developmental processes to test the second. They find moderate support for both hypotheses and present a comprehensive theory of girls' developmental psychopathology that integrates social and developmental influences.

Vocal learners such as humans and songbirds can learn to produce elaborate patterns of structurally organized vocalizations, whereas many other vertebrates such as non-human primates and most other bird groups either cannot or do so to a very limited degree. To explain the similarities among humans and vocal-learning birds and the differences with other species, various theories have been proposed. One set of theories are motor theories, which underscore the role of the motor system as an evolutionary substrate for vocal production learning. For instance, the motor theory of speech and song perception proposes enhanced auditory perceptual learning of speech in humans and song in birds, which suggests a considerable level of neurobiological specialization. Another, a motor theory of vocal learning origin, proposes that the brain pathways that control the learning and production of song and speech were derived from adjacent motor brain pathways. Another set of theories are cognitive theories, which address the interface between cognition and the auditory-vocal domains to support language learning in humans. Here we critically review the behavioral and neurobiological evidence for parallels and differences between the so-called vocal learners and vocal non-learners in the context of motor and cognitive theories. In doing so, we note that behaviorally vocal-production learning abilities are more distributed than categorical, as are the auditory-learning abilities of animals. We propose testable hypotheses on the extent of the specializations and cross-species correspondences suggested by motor and cognitive theories. We believe that determining how spoken language evolved is likely to become clearer with concerted efforts in testing comparative data from many non-human animal species.

Understanding the neural basis of social communication and vocal perception in primates is a key challenge in systems neuroscience. Vocalizations are fundamental for communication, and several cortical areas, known as "voice patches," have been identified as being sensitive to conspecific vocalizations in primates, vital for distinguishing species-specific calls. While the dorsal stream's role in complex auditory-motor functions and human speech processing is established, its specific contribution to processing species-specific vocalizations in non-human primates remains unclear. Using high-resolution fMRI (0.6 mm isotropic voxels), we investigated brain regions involved in processing vocalizations in awake rhesus monkeys exposed to coos, screams, and aggressive calls, among control sounds. Our analyses revealed a widespread network involved in vocalization processing, encompassing auditory-associated areas including the core and belt auditory cortices, as well as premotor, and somatosensory-related areas. Moreover, we found selective activation in the caudal part of the lateral sulcus (area Tpt) and the dorsal premotor cortex (area 6DR/F2) in response to vocalizations. Also, the population responses in these areas could discriminate between different vocalizations. Our results enhance our understanding of the neural basis of vocal communication in primates. Specifically, they highlight the involvement of a voice-related dorsal network in macaques, including Tpt and part of 6DR/F2, in processing the acoustic features of salient vocal stimuli, potentially linking them to motor representations. These findings provide insights into potential evolutionary precursors of auditory-motor pathways that support complex auditory communication systems in primates, including human speech.